Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The balance between RuBP carboxylation and RuBP regeneration: a mechanism underlying the interspecific variation in acclimation of photosynthesis to seasonal change in temperature

Yusuke Onoda A B D , Kouki Hikosaka A and Tadaki Hirose A C

A Graduate School of Life Sciences, Tohoku University, Aoba, Sendai, 980-8578 Japan.

B Current address: Department of Plant Ecology, Utrecht University, PO Box 800.84 3508 TB Utrecht, The Netherlands.

C Department of International Agriculture Development, Tokyo University of Agriculture, Sakuragaoka 1-1-1, Setagaya, Tokyo, 156-8502 Japan.

D Corresponding author. Email: Y.Onoda@bio.uu.nl

Functional Plant Biology 32(10) 903-910 http://dx.doi.org/10.1071/FP05024
Submitted: 31 January 2005  Accepted: 20 May 2005   Published: 5 October 2005

Abstract

The ratio of the capacities of ribulose-1,5-bisphosphate (RuBP) regeneration to RuBP carboxylation (Jmax / Vcmax) (measured at a common temperature) increases in some species when they are grown at lower temperatures, but does not increase in other species. To investigate the mechanism of interspecific difference in the response of Jmax / Vcmax to growth temperature, we analysed the temperature dependence of Vcmax and Jmax in Polygonum cuspidatum and Fagus crenata with the Arrhenius function. P. cuspidatum had a higher ratio of Jmax / Vcmax in spring and autumn than in summer, while F. crenata did not show such change. The two species had a similar activation energy for Vcmax (EaV) across seasons, but P. cuspidatum had a higher activation energy for Jmax (EaJ) than F. crenata. Reconstruction of the temperature response curve of photosynthesis showed that plants with an inherently higher EaJ / EaV (P. cuspidatum) had photosynthetic rates that were limited by RuBP regeneration at low temperatures and limited by RuBP carboxylation at high temperatures, while plants with an inherently lower EaJ / EaV (F. crenata) had photosynthetic rates that were limited solely by RuBP carboxylation over the range of temperatures. These results indicate that the increase in Jmax / Vcmax at low growth temperatures relieved the limitation of RuBP regeneration on the photosynthetic rate in P. cuspidatum, but that such change in Jmax / Vcmax would not improve the photosynthetic rate in F. crenata. We suggest that whether or not the Jmax / Vcmax ratio changes with growth temperature is attributable to interspecific differences in EaJ / EaV between species.

Keywords: activation energy, interspecific variation, Jmax, temperature acclimation, Vcmax.


References

Bernacchi CJ Singsaas EL Pimentel C Portis AR Jr Long SP 2001 Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell & Environment 24 253 259

Berry J Björkman O 1980 Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31 491 543
DOI

Bunce JA 2000 a Acclimation of photosynthesis to temperature in eight cool and warm climate herbaceous C3 species: temperature dependence of parameters of a biochemical photosynthesis model. Photosynthesis Research 63 59 67 DOI

Bunce JA 2000 b Acclimation to temperature of the response of photosynthesis to increased carbon dioxide concentration in Taraxacum officinale. Photosynthesis Research 64 89 94 DOI

Drake BG Gonzalez-Meler MA Long SP 1997 More efficient plants — a consequence of rising atmospheric CO2. Annual Review of Plant Physiology and Plant Molecular Biology 48 609 639 DOI

Dreyer E Le Roux X Montpied P Daudet FA Masson F 2001 Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiology 21 223 232

Ethier GJ Livingston NJ 2004 On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model. Plant, Cell & Environment 27 137 153
DOI

Evans JR 1987 The relationship between electron transport components and photosynthetic capacity in pea leaves growth at different irradiances. Australian Journal of Plant Physiology 14 157 170

Farquhar GD von Caemmerer S Berry JA 1980 A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149 78 90
DOI

Farquhar GD von Caemmerer S 1982 Modelling of photosynthetic response to environmental conditions. In ‘Physiological plant ecology II’. Lange OL Novel PS Osmond CB Ziegler H 550 587 Springer-Verlag Heidelberg

Fridlyand LE Backhausen JE Scheibe R 1999 Homeostatic regulation upon changes of enzyme activities in the Calvin cycle as an example for general mechanisms of flux control. What can we expect from transgenic plants? Photosynthesis Research 61 227 239 DOI

Harrison EP Olcer H Lloyd JC Long SP Raines CA 2001 Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubisco carboxylation capacity. Journal of Experimental Botany 52 1779 1784 DOI

Hikosaka K 1997 Modelling optimal temperature acclimation of the photosynthetic apparatus in C3 plants with respect to nitrogen use. Annals of Botany 80 721 730 DOI

Hikosaka K 2005 Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves grown at different temperature and light conditions: similarities and differences between temperatures and light acclimation. Plant and Cell Physiology (In press)

Hikosaka K Murakami A Hirose T 1999 Balancing carboxylation and regeneration of ribulose-1,5-bisphosphate in leaf photosynthesis: temperature acclimation of an evergreen tree, Quercus myrsinaefolia. Plant, Cell & Environment 22 841 849 DOI

Kirschbaum MUF Farquhar GD 1984 Temperature dependence of whole-leaf photosynthesis in Eucalyptus pauciflora Sieb. ex Spreng. Australian Journal of Plant Physiology 11 519 538

Loreto F Dimarco G Tricoli D Sharkey TD 1994 Measurement of mesophyll conductance, photosynthetic electron transport and alternative electron sinks of field grown wheat leaves. Photosynthesis Research 41 397 403


Medlyn BE Loustau D Delzon S 2002 a Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.). Plant, Cell & Environment 25 1155 1165
DOI

Medlyn BE Dreyer E Ellsworth D Forstreuter M Harley PC et al 2002 b Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment 25 1167 1179 DOI

Muraoka H Koizumi H 2005 Photosynthetic and structural characteristics of canopy and shrub trees in a cool-temperate deciduous broadleaved forest: implication to the ecosystem carbon gain. Agricultural and Forest Meteorology (In press)

Nie GY Long SP Garcia RL Kimball BA Lamorte RL Pinter PJ Jr Wall GW Webber AN 1995 Effects of free-air CO2 enrichment on the development of the photosynthetic apparatus in wheat, as indicated by changes in leaf proteins. Plant, Cell & Environment 18 855 864


Onoda Y Hikosaka K Hirose T 2005 Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum. Journal of Experimental Botany 56 755 763
DOI

Price GD von Caemmerer S Evans JR Siebke K Anderson JM Badger MR 1998 Photosynthesis is strongly reduced by antisense suppression of chloroplastic cytochrome bf complex in transgenic tobacco. Australian Journal of Plant Physiology 25 445 452

Sage RF 1994 Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspective. Photosynthesis Research 39 351 368
DOI

Sharkey TD Stitt M Heineke D Gerhardt R Raschke K Heldt HW 1986 Limitation of photosynthesis by carbon metabolism II. O2 insensitive CO2 assimilation results from triose phosphate utilization limitations. Plant Physiology 81 1123 1129

Sudo E Makino A Mae T 2003 Differences between rice and wheat in ribulose-1,5-bisphosphate regeneration capacity per unit of leaf-N content. Plant, Cell & Environment 26 255 263
DOI

Terashima I Evans JR 1988 Effect of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant & Cell Physiology 29 143 156

Theobald JC Mitchell RAC Parry MAJ Lawlor DW 1998 Estimating the excess investment in ribulose-1,5-bisphosphate carboxylase / oxygenase in leaves of spring wheat grown under elevated CO2. Plant Physiology 118 945 955
DOI

von Caemmerer S 2000 ‘Biochemical models of leaf photosynthesis.’ CSIRO Publishing Melbourne

von Caemmerer S Farquhar GD 1981 Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153 376 387 DOI

Walcroft AS Whitehead D Silvester WB Kelliher FM 1997 The response of photosynthetic model parameters to temperature and nitrogen concentration in Pinus radiata D. Don. Plant, Cell & Environment 20 1338 1348 DOI

Wilson KB Baldocchi DD Hanson PJ 2000 Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiology 20 565 578

Wullschleger SD 1993 Biochemical limitations to carbon assimilation in C3 plants: a retrospective analysis of the A / Ci curves from 109 species. Journal of Experimental Botany 44 907 920


Yamasaki T Yamakawa T Yamane Y Koike H Satoh K Katoh S 2002 Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in Winter wheat. Plant Physiology 128 1087 1097
DOI

Yamori W Noguchi K Terashima I 2005 Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions. Plant, Cell & Environment 28 536 547 DOI



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